457 ARTICLE Patterns of genome size diversity in bats (order Chiroptera)1 Jillian D.L. Smith, John W. Bickham, and T. Ryan Gregory Abstract: Despite being a group of particular interest in considering relationships between genome size and metabolic param- eters, bats have not been well studied from this perspective. This study presents new estimates for 121 “microbat” species from 12 families and complements a previous study on members of the family Pteropodidae (“megabats”). The results confirm that diversity in genome size in bats is very limited even compared with other mammals, varying approximately 2-fold from 1.63 pg in Lophostoma carrikeri to 3.17 pg in Rhinopoma hardwickii and averaging only 2.35 pg ± 0.02 SE (versus 3.5 pg overall for mammals). However, contrary to some other vertebrate groups, and perhaps owing to the narrow range observed, genome size correlations were not apparent with any chromosomal, physiological, flight-related, developmental, or ecological characteristics within the order Chiroptera. Genome size is positively correlated with measures of body size in bats, though the strength of the relation- ships differs between pteropodids (“megabats”) and nonpteropodids (“microbats”). Key words: Chiroptera, genome size, C-value, flight, metabolism. Résumé : Bien qu’elles constituent un groupe présentant un intérêt particulier pour l’étude des relations entre la taille du génome et les paramètres métaboliques, les chauves-souris n’ont pas été bien étudiées sous cet angle. Dans ce travail, les auteurs présentent des estimés pour 121 espèces de “microchiroptères” appartenant a` 12 familles et ceci vient compléter une étude antérieure sur des membres de la famille des Pteropodidae (“mégachiroptères”). Les résultats confirment que la diversité de la taille des génomes chez les chauves-souris est limitée par rapport a` d’autres mammifères, variant environ du simple au double entre 1,63 pg chez le Lophostoma carrikeri a` 3,17 pg chez le Rhinopoma hardwickii pour une moyenne de 2,35 pg ± 0,02 (contre 3,5 pg globalement chez les mammifères). Cependant, contrairement a` ce qui est observé chez d’autres vertébrés, peut-être en raison de la faible variation observée, la taille du génome ne semblait pas corrélée avec des caractéristiques chromosomiques, physio- logiques, liées au vol, développementales ou écologiques chez les chiroptères. La taille du génome était cependant positivement corrélée avec divers paramètres de la taille du corps chez les chauves-souris, bien que le degré de corrélation différait chez les ptéropodidés (“mégachiroptères”) et les non-ptéropodidés (“microchiroptères”). [Traduit par la Rédaction] Mots-clés : Chiroptera, taille du génome, valeur C, vol, métabolisme. For personal use only. Introduction 132.83 pg), especially with the objective of identifying phenotypic The order Chiroptera is the second largest in mammals after correlates that could help to explain this astounding diversity rodents, and with >1100 species in 18 families it represents more (Gregory 2013). However, increasing attention has been paid more than one-fifth of all mammalian diversity (Wilson and Reeder recently to explaining the apparent constraint within some 2005). While bats share many commonalities with other mam- otherwise diverse vertebrate taxa, in particular among birds mals, they are the only mammals capable of true flight and, along (Andrews et al. 2009). with birds and the extinct pterosaurs, one of only three vertebrate It has been hypothesized that genome size may be constrained in taxa to have evolved this highly specialized mode of locomotion. some vertebrate groups with high metabolic rates. This is particu- Despite their diversity, abundance, and unique biology, bats re- larly relevant in those taxa subject to the extreme metabolic de- main poorly studied from several important perspectives. Nota- mands of powered flight owing to the relationship between genome bly, research into the diversity of genome size in bats is one such size, cell size, and mass-specific metabolic rate (Hughes and Hughes area that is lacking. Prior to recent work by the current authors 1995; Gregory 2002a; Organ and Shedlock 2009). Specifically, smaller Genome Downloaded from www.nrcresearchpress.com by 65.74.4.35 on 01/25/16 (J.D.L. Smith and Gregory 2009; present study), estimates available cells—which are associated with small genomes—have a higher sur- in the Animal Genome Size Database covered only 62 species from face area to volume ratio, allowing for improved gas exchange to 7 families (Gregory 2013). meet metabolic demands (Szarski 1983; Gregory 2001b). In one analysis, Hughes (1999) used a comparatively small data- Genome size constraint set for birds to suggest that strong flyers have smaller genomes The genome sizes of animals as a whole range more than 7000-fold. than weak flyers or flightless taxa (see also Gregory (2005a)). More Even among vertebrates, genome sizes vary by a factor of more recently, Andrews et al. (2009) used a much larger, newly gener- than 350. Not surprisingly, many studies on genome size in ani- ated dataset to examine the relationship between genome size mals have focused on groups with large amounts of variability, and flight using specific wing parameters. In this case, genome such as amphibians (1C = 0.95 – 120.60 pg) and “fishes” (1C = 0.35 – size was positively correlated with wing loading index (an inverse Received 8 March 2013. Accepted 8 July 2013. Corresponding Editor: Jillian Bainard. J.D.L. Smith and T.R. Gregory. Department of Integrative Biology, University of Guelph, 50 Stone Road E., Guelph, ON N1G 2W1, Canada. J.W. Bickham. Battelle Memorial Institute, 10777 Westheimer, Suite 1105, Houston, TX 77042, USA. Corresponding author: T. Ryan Gregory (e-mail: [email protected]). 1This article is one of a selection of papers published in this Special Issue on Genome Size Evolution. Genome 56: 457–472 (2013) dx.doi.org/10.1139/gen-2013-0046 Published at www.nrcresearchpress.com/gen on 23 September 2013. 458 Genome Vol. 56, 2013 indicator of flight efficiency) in passerine birds, lending support velopmental traits have also been studied in fishes, birds, and to the flight constraint hypothesis (Andrews et al. 2009). Fossil mammals (including within primates and rodents), although re- evidence also shows that avian dinosaurs and pterosaurs had ports have been conflicting with no clear indication of its impor- small genomes relative to nonflying lineages (Organ et al. 2007; tance to genome size (Morand and Ricklefs 2001, 2005; Gregory Organ and Shedlock 2009). In light of these studies on other flying 2002c; E.M. Smith and Gregory 2009). vertebrates, it seems that flight may indeed impose a constraint It might be tempting to assume that because links have been on genome size. Clearly, a study of bats also represents a critical found between genome size and one or more adaptive characters, component of this line of inquiry. that this alone may be responsible for observed diversity in DNA amount among species. However, there are nonadaptive possibil- Explaining genome size diversity within bats ities that should also be considered. For example, it is possible While genome size in bats appears constrained based on the lim- that mutational processes at the level of whole chromosomes play ited sampling conducted to date, little is known about the causes and an important role. Indeed, a link has been found between genome consequences of this variation. Flight is a proposed constraint on size and chromosomal number in teleost fishes (Mank and Avise genome size; however, previous studies have not considered rela- 2006; E.M. Smith and Gregory 2009). Whether genome size is driven tionships between genome size and flight or any other organism by chromosomal duplications or losses, or whether more DNA is level traits within Chiroptera, such that work on this group lags associated with higher rates of breakage, remains an open issue. It is, behind that focusing on other vertebrates (reviewed in Gregory therefore, worth examining these associations in bats and other 2005a). Mammals, like birds, demonstrate strong positive links be- groups. tween genome size and cell size and inverse relationships between Another intriguing possibility relates genome size to mutation genome size and metabolic rate (Vinogradov 1995; Gregory 2000). In rate, genetic drift, and population size. From the perspective of some cases, relationships can be identified within individual orders, population genetics, smaller populations are more susceptible to such as a correlation between genome size and body size in rodents the influence of genetic drift, and thus the genomes of these (Gregory 2002c) or between genome size, cell size, and flight param- animals are more likely to retain mildly deleterious mutations. eters within the avian order Passeriformes (Andrews et al. 2009). Lynch and Conery (2003) proposed that animals have larger ge- It, therefore, remains an important question whether cell- and nomes relative to prokaryotes and unicellular organisms because organism-level traits, especially those relevant to flight, are related to their smaller population sizes passively allowed for the accumu- genome size diversity among bats; and whether this can help to lation of gene duplications and mobile genetic elements. While explain patterns within this highly diverse mammalian order, in empirical support for this model has been limited (Gregory and addition to assessing the larger issue of flight-related constraints Witt 2008), this remains a question